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Notice: ©1988 Springer. This manuscript is an author version with the final publication available at http://www.springerlink.com and may be cited as: Gustafson, R. G., & Reid, R. G. B. (1988). Larval and post‐larval morphogenesis in the gutless protobranch bivalve Solemya reidi (Cryptodonta: Solemyidae). Marine Biology, 97(3), 373‐387. doi:10.1007/BF00397768

Marine Biology 97,373-387 (1988) Marine

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,.­ Larval and post-larval morphogenesis in the gutless protobranch bivalve Solemya reidi (Cryptodonta: Solemyidae) ~:~

R. G. Gustafson ':,,:' and R. G. B. Reid

Department of Biology, University of Victoria, Victoria, British Columbia V8W 2Y2, Canada

Abstract the extreme reduction of the alimentary tract in species of Solemva (Pelseneer 1891. Sternpell 1899, Yonge 1939, Owen Structural changes occurring In the alimentary tract, 1959,1961), but the above studies were the first to indicate perivisceral cavity, foot, hypobranchial gland, and gills of that some members of the protobranch bivalve-subclass larval and post-larval Solemya reidi, a gutless protobranch Cryptodonta, containing the order Solemyoida and the ex­ bivalve, were examined using both light and electron mi­ tant families Solemyidae and Nucinellidae, totally lacked a croscopy at I. 3, 5, 18, 34 and 42 d after fertilization, A ful­ digestive tract. ly developed mouth, esophagus, and anus, together with Other gutless marine invertebrates are found among the rudiments of a stomach and rectum are present before the Nematoda (Ott et al. 1982), Polychaeta (louin 1979), metamorphosis, At metamorphosis, the cells making up the Oligochaeta (Richards et al. 1982), Turbellaria (Ott et al. dorsal and lateral walls of the stomach dissociate, and by 1982), and in all Pogonophora (Ivanov 1963), With the ex­ 18 d the mouth and anus are the only remaining portions ception of pogonophorans (Gureeva and Ivanov 1986), of the alimentary tract. The larval test is ingested into the nothing is known concerning formation of the gutless con­ perivisceral cavity at metamorphosis and its autolysis con­ dition or fate of the endoderm in these organisms, tinues through at least the 42nd day after fertilization, The An understanding of the formation of the gutless con­ foot, gills, and hypobranchial gland, poorly developed at dition in solemyoid protobranchs depends on detailed metamorphosis, develop slowly and are still undergoing knowledge of early development and organogenesis. Two extensive morphogenesis at 42 d. studies have dealt with nuculoid protobranchs; Nucula de!­ phinodonta Mighels (Drew 190I) and Yo!dia limatula Say (Drew 1899a), Less detailed information was provided for N. proxima Say (Drew 1899 b, 190I), Individuals of the Introduction genus Nucula previously referred to N. proxima are com­ posed of two species, N. proxima and N. annu!ata Hamp­ The discovery that adult specimens of the solemyoid bi­ son, 1971 (Hampson 1971), The purpose of the present valves Solemva reidi Bernard, 1980 (Reid 1980, Reid and study is to provide information on larval and post-larval Bernard 1980), S. borealis Totten (Reid and Bernard 1980), organogenesis in Solemya reidi that will contribute to Petrasma atacama Kuznetsov and Shileiko, 1984, Acharax understanding the fate of the endoderm in this and other eremita Kuznetsov and Shileiko, 1984, and Nucinella gutless bivalves. maxima Thiele and Jaeckel (Kuznetsov and Shileiko 1984) lack an alimentary tract raised questions concerning mor­ phogenesis of this gutless condition and the consequent Materials and methods fate of gut-forming endodermal tissues during devel­ opment (Gustafson and Reid 1986), Workers remarked on Larval and post-larval Solemya reidi were cultivated through metamorphosis at Day 6 until 42 d after fertili­ zation, The collecting site and culture techniques have * Harbor Branch Oceanographic Institution Contribution been described (Gustafson and Reid 1986), No. 601. Larvae and post-larvae were fixed at intervals of I, 3, 5, ** Present address: Division of Applied Biology, Harbor Branch 18,34 and 42 d after fertilization, All developmental stages Oceanographic Institution, 5600 Old Dixie Highway, Fort Pierce, Florida 34946, USA were fixed for transmission and scanning electron mi- 374 R. G. Gustafson and R. G. B. Reid: Gutless bivalve morphogenesis croscopy in a solution of 2% glutaraldehyde, 0.2 M phos­ mantle margins are evident (Figs. 11-13). These problem­ phate buffer, and 0.14 M NaCI at pH 7.3, followed by three atic cells, four in either mantle margin and containing a rinses in 0.2 M phosphate buffer combined with 0.28 M large central vacuole, were first seen at 3 d and eventually NaCL and post-fixation in 2% OS04 in 1.25% NaHCO,. Af­ come to lie in the extreme anterior portion of the mantle ter fixation, specimens were dehydrated in alcohol. Further by Day 18 (Fig. II). They histolyze soon thereafter. By this preparation of specimens for microscopy has been de­ time, the foot has grown considerably, emphasizing the scribed by Gustafson and Reid (1986). Serial, longitudinal. longitudinal division of the sole; the gill buds are more and cross-sections of each stage were used to determine in­ prominent: the ciliated cells posterior to the foot. rep­ ternal morphology. resenting a portion of the presumptive hypobranchial gland, have expanded; and the epithelial region around the mouth is more heavily ciliated than at metamorphosis Results (Fig. 14). The foot is now active and often extends beyond the limits of the mantle cavity. Specimens did not crawl or Internal larval morphology burrow. TIle anterior adductor muscle forms before the posterior. By Day 34, gill filaments are present. the foot is In Solemya reidi, boundaries between germ layers are dif­ muscularized, and the mass of ingested larval test cells are ficult to discern in I d larvae due to compression of the ar­ evident within the perivisceral cavity (Figs. 15, 16). chenteron lumen and to close apposition of cell layers (Figs. 1-4). In longitudinal section (Figs. 1,2), a distinction can be made between ciliated test (comprised of larval ec­ Alimentary tract toderm), elongated cells comprising the shell field, a group offour anterior definitive ectoderm cells, the rest of the de­ TIle developing esophagus was first detected in TEM sec­ finitive adult ectoderm, and the central mass of endoderm. tion at 3 d post-fertilization as a small group of ciliated Development of larval shell and definitive adult organs of cells in the anterior visceral mass, ventral to the periviscer­ S. reidi occurs within and is obscured by the test. The shell al cavity (Fig. 17). By Day 5, the walls of the esophageal field gives rise to the mantle, which will subsequently se­ tube were heavily lined with cilia (Fig. 18). While the eso­ crete the shell. The fate of the anterior quartet of ectoderm phagus is continuous with the mouth of pre- and post­ cells, located at the base of the cephalic plate where the an­ metamorphic larvae and juveniles, the esophageal lumen terior definitive ectoderm comes in contact with the base of was never seen to connect with the stomach rudiment. Fol­ the first row of larval test cells, will be more fully discussed lowing metamorphosis, and dissociation of the stomach below ("Discussion - Nervous system"). rudiment. the esophagus connects directly with the lumen Early in development. the test and definitive tissues are of the perivisceral cavity (Fig. 19). The esophagus was not closely applied (Figs. 1-4), but by the third day a space de­ recognizable in light microscopy sections of 18, 34 or 42 d velops between these two tissues (Figs. 5-10). Mantle, sto­ juveniles: its dissolution occurs rapidly following metamor­ madeurn, perivisceral cavity, and stomach rudiment are phosis. evident at this stage (Figs. 5-10). Although the mantle is The presumptive lumen of the stomach, first recogniz­ fully elaborated, no evidence of shell mineralization, in­ able as an array of tightly packed microvilli, lies within a dicated by birifringence under polarized light, was detect­ cylinder of cells representing the mid-gut rudiment and ex­ ed in larval specimens. A shell field invagination was not tends the length of the mid-ventral region of the periviscer­ observed. The ventral stomadeum runs from the vicinity of al cavity (Figs. 7-10 and 20-22). In some specimens, the the "pseudo-blastopore" (see Gustafson and Reid 1986) to walls of the stomach separate forming an elongated cylin­ the vicinity of the stomach rudiment. A large lumen rep­ dricallumen (Fig. 23) lined with microvilli (Fig. 24), which resenting the perivisceral cavity is bounded ventrally by may be homologous with tightly packed microvilli seen in visceral mass and dorsally and laterally by mantle. The the stomach rudiment (Fig. 22). No stomach ciliation was stomach or mid-gut rudiment lies within the perivisceral found. cavity. The rectal rudiment is apparent on the fifth day of development. A small tuft of cilia protrudes from the anal opening, which extends into the non-functioning rectal Post-larval morphology rudiment (Fig. 25). The stornadeum, observed in sections of 3 d larvae (Figs. 5, 6), is quickly resorbed and is not ap­ By 18 d after fertilization, anterior and posterior adductor parent in later larvae or juveniles. Its confluence with the muscles, as well as eight problematic cells in the anterior pseudo-blastopore cavity and derivation from larval ec-

Figs. 1-4. Solemva reidi. 1: Light micrograph of I I'm longitudinal section of ld pericalymma larva: dorsal is to the bottom (scale bar= 100 I'm). 2: Diagrammatic depiction ofsection shown in Fig. I (same scale). 3: Light micrograph of l,um cross-section through pos­ terior region of Id pericalymma larva (scale bar = 50 I'm). 4: Diagrammatic depiction of section shown in Fig. 3 (same scale). ant: an­ terior; aq: anterior quartet; ar: archenteron; bp: blastopore; de: definitive ectoderm; en: endoderm; pos: posterior; sf: shell field; tc: test cell CD

R. G. Gustafson and R. G. B. Reid: Gutless bivalve morphogenesis 377 toderm could not be verified. During metamorphosis, cells cytoplasm and nucleus of these mucous cells occupy a pe­ comprising the dorsal and lateral walls of the stomach or ripheral position, while the center contains a structureless mid-gut rudiment dissociate and any test material ingested electron-lucent mass traversed by dense filamentous at metamorphosis is released directly into the perivisceral strands (Fig. 34). The fibrillar mucus is arranged either as cavity (Fig. 26). granules or as structureless accumulations of mucus, prob­ Ingestion of test begins as early as Day 5, at least one ably resulting from breakdown of the walls of the mucous full day before metamorphosis has begun and while the granules (Fig. 34). Another dense homogeneous secretion pericalymma larva is still in the water column (Fig. 27). is present in some mucous cells (Fig. 35). Many small However. this involves only a portion of the basal region of fibrillar mucous granules can be seen in the vicinity of Gol­ the test cells, the majority of the test being ingested follow­ gi apparatuses (Fig. 36). ing metamorphosis.

Gills Foot The gill primordia consist of two gill buds or papillae, The foot is first seen in recently metamorphosed juveniles which protrude from the mantle walls on either side of the as a bilobed protuberance in the mid-section of the mantle mantle cavity directly posterior to the base of the foot. cavity, attached dorsally to the visceral mass. The lateral Poorly developed at metamorphosis, the gill buds are still distal surfaces of the foot are ciliated and the opening to rudimentary 15 d after fertilization (Figs. 37,38). By 18 d, the pedal gland duct is present in the mid-ventral portion the ventral surfaces of the gill buds are heavily ciliated and of the foot. As the foot grows, the two lateral lobes separate filaments are beginning to form (Fig. 39). and grow further apart (Fig. 28), leading eventually to the By 34 d after fertilization, several filaments are present broad flattened sole characteristic of adult protobranch bi­ in each gill bud (Fig. 40). Filaments form by transverse valves. By Day 15, a single protuberance is apparent at the splitting of the gill bud. A lack of specimens precluded a base of the ventral surface of each lobe of the foot (Fig. 28). more detailed study ofgill formation. Furrows or pleats on the lateral edges of the foot appear by Day 34 (Figs. 15, 16) and develop into the papillae which border the sole in adult Solemya reidi. The anterior pa­ Nervous system pillae form first, while subsequent ones are added pos­ teriorly. Although organogenesis of the nervous system in Solemya TI1e primordial pedal gland is first discerned on Day 5 reidi could not be traced with confidence, the anterior as a group of reticulated cells deep in the center of the foot. quartet of definitive ectodermal cells (Figs. 41, 42) may A ciliated duct leads from the pedal gland to the mid-line represent the presumptive cerebral ganglion. The cerebral of the ventral surface of the foot, where it emerges as a ganglion itself was first observed in juveniles 34 d old large pore (Fig. 28). The pedal gland ramifies throughout (Figs. 15,16). the middle region of th e foot and is com posed of mucus-se­ creting cells, containing both an electron-lucent fibrillar mucus substance and a denser, homogeneous secretion Discussion (Figs. 29-32). Alimentary tract

Presumptive hypobranchial gland Larvae and recently metamorphosed juveniles of Solemya reidi possess a well developed mouth, esophagus, and Mucous glands are located laterally in the posterior mantle anus; together with rudiments of the mid-gut and hind-gut. epithelia of Solemya reidi by 18 d after fertilization The mouth and esophagus are the only functional organs (Figs. 11,33). These glands, lying to either side ofa band of of the digestive tract; they assist in engulfment of portions ciliated cells (Fig. 33), may be homologous with the adult of the test. Other components of the digestive tract are ves­ hypobranchial gland. The hypobranchial gland in adult tigial. Structures identifiable as digestive diverticula or S. reidi is a mucus-secreting organ lining the dorsolateral style sac were not seen. inner surface of the mantle, as well as both sides of the cte­ In both the Solemyidae and the Nucinellidae, the size nidial axes in the posterior region of the mantle cavity. The of the gut is reduced from a simple but probably functional

.. Figs. 5-10. Solemya reidi. 5: Light micrograph of l rzrn cross-section through anterior of 3 d pericalymma larva (scale bar= 50 ,um; valid for Figs. 5-10). 6: Diagram of section shown in Fig. 5. 7: Light micrograph of I ,urn cross-section through mid-section of 3 d pericalymma larva. 8: Diagram of section shown in Fig. 7. 9: Light micrograph of I ,um cross-section through posterior region of 3 d pericalymma larva. 10: Diagram of section shown in Fig. 9. rna: mantle; pv: perivisceral cavity; sl: stomach lumen; sp: space separating test and definitive tissues; sr: stomach rudiment; st: stomadeum; tc: test cell cb .\

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Figs. 11-14. Solemya reidi . II. Light micrograph of I pm cross-section of posterior porti on of 18 d j uve nile (scale bar = 50 pm); ventral is to bottom in Figs. 11- l3. 12: Light micrograph of 1pm cross-section of 18d juvenile anterior to that depic ted in Fig. I I (sam e scale). 13: Light micrograph of I pm cross-section of anterior porti on of 18 d juvenile (sa me scale as in Fig. I I). 14: SEM of gaping 15d juvenile, showing structures within mantle cavity; arrow indicate s site of pedal gland opening (scale bar= 25 p m). aa : anterior adductor ; ant: an­ terior : cb : band of cilia; f: foot ; gb : gill bud ; rna: mantle; me: mantle cavity; mg: mantle mu cou s gland; mo: mouth; pa : posterior ad­ du ctor; pos: posteri or; tc: inges ted test ma teria l in perivisceral cavity ; va : vacuole in problematic cell f ,

..

® Figs. 15, 16. Solemya reidi. 15: Light micrograph of I ~m longitudinal section th rou gh 34d j uve nile. 16: Diagram of section shown in Fig. 15. Dorsal is at bott om in figures. and both are to same sca le; sca le bar = 100 Jim . aa: anter ior adducto r; ant: anterior; cg: cerebral ganglion; f: foot; gb: gill bud; rna: mant le; mc: mantle cav ity ; pa : posteri or adductor; pos: poster ior; tc: inges ted test cells in perivisceral cavity , ,

..

Figs. 17-22. So lemya reidi. 17: TE M showi ng pr im o rd ium of eso phagus in 3 d pe rica lyrnma larva : ciliogenesis has begun a nd lumen of th e eso phagus is form ing. as the wall s (ar ro ws ) of th e pr im ord iu m separate ( ~ c a le bar = 2.5 p m). 18: TEM of transverse section th rou gh lum en of cilia ted esophagu s in a 5 d pericalymrna larv a (scale bar = 5/lm ). 19: Light m icrograp h of longi tud ina l section th rou gh eso phagus of post-rnetam o rpluc. 7 d j uve nile (scal e bar = 20 p m ). 20: Light microgra ph of 1pm cross-sec tion throug h sto ma ch rudiment in 3 d pe rica lym ma lar va sh owing pr imordium ofsto mach lum en ( 51) (scal e ba r = 10 /lm). 21: Light micr ogra ph or I pm longitudinal section th rou gh 5 d pericalymma la rva. showing sto mach rudiment (sf) a nd portion o f th e eso phag us (e) (scal e ba r = 25/l m ). 22: T EM show ing fine-str uc tu re o f putati ve mi crovilli occ u pying future lum en o f th e stomach rudi me nt in 5 d pe ricalyrnma la rva (scal e bar= 0.25 pm). el. eso phagus lumen: m : m itoc hondria: nu : nu cleu s of endo derm ce ll: pv: pe rivisce ra l cav ity R.G. Gustafson and R. G. B.Reid: Gutless bivalve morphogenesis 381 system as described for Solemya togata (Poli (Yonge 1939), recognized its significance. This cavity can be traced back S. velesiana (Iredale) (Reid and Brand 1987), and Nucinella to the blastocoel in lamellibranch bivalves (D'Asaro 1967). serrei Lamy (Allen and Sanders 1969) through the vestigial Derivation of the perivisceral cavity from a persistent condition as seen in S. parkinsoni Smith (Owen 1961), blastocoel would necessarily classify it as a pseudocoel and S. australis Lamarck (Reid and Brand 1987), and N. viri­ not a true coelom. The perivisceral cavity of protobranch dula (Kuznetsov and Shileiko 1984) to its total loss in bivalves appears to have separate origin. As the shell field S. reidi, 51. borealis, (Reid and Bernard 1980), and spreads laterally and arches dorsally to form the mantle, a N. maxima (Kuznetsov and Shileiko 1984). The presence of large perivisceral cavity forms between it and the alimen­ fully elaborated, although in some cases miniscule, guts in tary canal in Nucula proxima, N. delphinodonta, Yo/dia /i­ members of both the Nucinellidae (Allen and Sanders matulu (Drew 1899a, b, 1901), and Solemya reidi. Drew 1969) and the Solemyidae (Pelseneer 1891, Sternpcll 1899, (1901) stated that the blastocoel disappears completely and Yonge 1939, Owen 1959, 1961, Bernard 1980, Reid and that the "space dorsal to the alimentary canal" represents a Bernard 1980, Reid and Brand 1987) suggest that the gut­ schizocoel of separate derivation. A blastocoelic cavity was less condition has arisen independently in these two closely never observed during development in 51. reidi. related families. Dissociation of the lateral and dorsal walls of the stom­ ach at metamorphosis in Solemya reidi also occurs in nu­ Foot culoid protobranchs (Drew 1899a, b. 1901). TI1e digestive diverticula and stomach walls reform within several days Despite the statement by Yonge (1962) that larvae of the following metamorphosis in the nuculoids (Drew 1901). genera Yo/dia and Nucula possess a functional byssus, Derivation of the gutless condition in adult S. reidi, nothing comparable to the byssal threads of lamellibranchs 51. borealis (Reid and Bernard 1980), Petrasma atacama, is secreted by either adult or larval protobranchs (Drew Acharax eremita. and Nucinella maxima (Kuznetsov and 1899 a, b, 190 L Allen and Sanders 1969, 1982, Allen 1985). Shileiko 1984) may ultimately be traced back to failure of Ultrastructure of the gland designated S' in the foot of portions of the gut to reform after dissociation at metamor­ Mvtilus edulis (Lane and Nott 1975, Lane et al. 1982) and phosis. 03 in the foot of Oslea edulis (Cranfield 1973) closely re­ scmblcs that of the single pedal gland ofjuvenile Solemya reidi (Figs. 31-33). The ultrastructural similarity between Perivisceral cavity these glands in lamellibranch pediveligers and juveniles of S. reidi may only indicate functional analogy in mucus se­ The existence of a prominent perivisceral cavity in bivalve cretion, but it does agree with the hypothesis that the pro­ larvae was emphasized by Elston (1980), but only D'Asaro tobranch pedal gland is ancestral to at least a portion of the (1967) and Drew (1899a, b, 1901) commented upon it or larnellibranch byssus gland (Yonge 1939, 1962).

Figs. 23-26. So!emya reidi. 23: Light micrograph of l/-lm longitudinal section of 5d pericalymma larva showing stomach lumen (sl) and perivisceral cavity; microvilli line walls of stomach lumen (scale bar = 25 ,um). 24: TEM showing detail of microvilli lining stomach lumcn in 5d pericalymma larva (scale bar= l/-lm). 25: TEM of longitudinal section through anus (an) of 5d pcricalymma larva (scale bar = 2.5 ,um). 26: Light micrograph of I urn longitudinal section of recently metamorphosed juvenile showing perivisceral cavity, inner opening of esophagus (e) and test cells (tc) entering perivisceral cavity via esophagus: dorsal is to top and anterior towards right (scale bar= 100/-lm). c: cilia: 1': foot: mv: microvilli; pv: perivisceral cavity: sp: space separating test and definitive tissues; t: test

Figs. 27-32. So!emya reidi. 27: Light micrograph of l/-lm section of 5d pericalymma larva showing detail of test cells being ingested (ar­ rowed) (scale bar = 50 /-lm). 28: SEM showing external view of foot in 15djuvenile: arrow indicates pedal gland opening; function and fate of the two ectodermal thickenings (ec). one on each lobe of the foot, is unknown (scale bar = 10,um). 29: Light micrograph of l jzrn cross-section showing extent of pedal gland (pg) development within foot of 18d juvenile (scale bar= 10 p.m). 30: TEM through portion of pedal gland of 18d juvenile showing mucous cells (mu) containing secretory material: between mucous cells are other, denser secretion materials (scale bar= 10lim). 31: TEM showing fine-structure of membranes within mucous cell of pedal gland of l8d juvenile (scale bar= I ,urn). 32: TEM showing fine-structure of dense secretory material and the secretory material (ms) which fills mucous cells of the pedal gland in 18d juvenile (scale bar= l zzm ), c: cilia: ds: dense secretory material: e: esophagus; me: mantle cavity; mo: mouth; n: nu­ cleus of mucous cell; sp: space separating test and definitive tissues; t: test: va: vacuole in problematic cell

Figs. 33-38. So!emya reidi. 33: Light micrograph of l/-lm cross-section of 18d juvenile at level of mantle mucous glands (mg): fibers of posterior adductor muscle (pa) are visible at bottom of micrograph; ventral is to the top (scale bar = 20 /-lm). 34: TEM of boundary be­ tween two secretory cells in mantle mucous gland of 42 d juvenile: individual fibrous mucous granules and structureless masses of mucus (fb) are present (scale bar= 5/-lm). 35: TEM of fine-structure of dense secretory material (ds) in mantle mucous gland of 18d juvenile (scale bar= I lim ). 36: TEM showing fine-structure of Golgi apparatuses (gc) within mucus-secreting cells of mantle mucous gland in 18d juvenile (scale bar= I pm). 37: SEM showing organs of posterior mantle cavity in 15djuvenile (scale bar = 10/-lm). 38: Scanning electron micrograph showing ciliated gill bud on right side of mantle cavity in 13d juvenile (scale bar= 5 11m). cb: band of cilia; 1': base of foot: gb: gill bud; gr: fibrous mucous granule; rna: mantle; me: mantle cavity; nu: nucleus

(Figs. 23-38 are on following pages) ·.

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384 R. G . G ustafso n a nd R. G . B. Reid : G utless bival ve mor ph ogenesis

, \' R.G . Gustafson a nd R. G . B. Reid ' G utless bivalve morphogenesis 385

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Figs. 39-42. S olemya reidi. 39: Light micrograph of I pm cross-section thro ugh posteri or ma ntl e cav ity a nd gill buds (gb) of 18d j uvenil e: ventra l is to right of microgra ph (sca le bar= 10 pm ). 40: Light m icrograph of I p mlongitudinal sectio n th rou gh gill bud of34djuvenile : gill bud has split int o severa l fila ments. leaving cilia ted furrows (arrow ed) bet wee n each filam en t; ventra l is to right (scale bar = 10 /Im) . 41: Light microgra ph of I p m cross-section o f I to 2d perica lymm a lar va in vici nity of co ntact bet ween a nte rior d efinitiv e ectod erm and base of first row of larval test cells; 4 cells (x) prese nt a t thi s point form the a nterio r qu artet of definiti ve ec tod erm ce lls (scale bar = 5 /I m ). 42: Light microgra ph o f I pm lon gitu din al sec tio n of I to 2 d pericalymma lar va a t sa me level as in Fig. 41 : 2 of th e 4 ante rio r ec tode rm cells are evident (scal e bar= 10 p m) . c: cilia ; ma: mantl e ; me: mant le cavity : na : anterior qu artet nuclei: nt : nucleus of test cell: tc: test cell ------

386 R. G. Gustafson and R. G. B.Reid: Gutless bivalve morphogenesis

Presumptive hypobranchial gland apical plate (Figs. 41, 42). These four cells may constitute the presumptive cerebral ganglia ofS. reidi. Mantle mucous glands located on opposite sides of the mantIc cavity directly posterior to the gill buds in juvenile Acknowledgements. We thank boat captains D. Horn, C. Dillen, Solemya reidi (Figs. 14,33) may represent primordia of the and S. Tueit for their able assistance in collecting Solemya reidi, B. Gustafson and D. Brand for assistance and perseverance in the adult hypobranchial gland. The ultrastructure of mucous field on many foul weather days, and Dr. R. D. Burke of the De­ gland cells in juvenile S. reidi (Figs. 34-36) is very similar partment of Biology, University of Victoria, for the use of his facili­ to that reported for hypobranchial gland of adult S. par­ ties for culturing larvae and juveniles. Special thanks also go to kinsoni (Morton 1977). In order to obtain the adult orienta­ D. Brand for preparation of the photographic plates. This research was supported by a University of Victoria Graduate Fellowship to tion of the hypobranchial gland, the mantle mucous glands the first author and an operating grant of the National Research of juvenile S. reidi must migrate dorsally and medially to Council of Canada to the second author. occupy the roof of the future suprabranchial chamber. The hypobranchial gland in adult S. reidi and S. parkinsoni oc­ cupies the external surfaces of the ctenidial axes and the surface of the dorsolateral aspect of the posterior mantle, Literature cited and is made up of unciliated mucous cells interspersed be­ Allen, J. A. (1985). The recent Bivalvia: their form and evolution. tween ciliated inversely conical cells (Morton 1977, Reid In: Trueman, E. R., Clarke, M. R. (eds.) The mollusca, Vol. 10. 1980). Evolution. Academic Press, New York, p. 337-403 Allen, J. A., Sanders, H. L. (1969). Nucinel/a serrei Lamy (Bivalvia: Protobranchia) a monomyarian solemyid and possible living actinodont. Malacologia 7: 381-396 Gills Allen, J. A., Sanders, H. L. (1982). Studies on the deep-sea Pro­ tobranchia; the subfamily Spinulinae (family Nuculanidae). Gill development in Solemya reidi is of the "simple" or Bull. Mus. compo Zoo I. Harv. 150: 1-30 "paleotaxodont type" (Raven 1966). Drew (1897, 1899a, b, Bcklcmishev, W. N. (1969). Principles of comparative anatomy of invertebrates, Vol. I and 2, [Transl. from Russian by J. M. 190I) pictures the mantle thickenings (gill buds) in Yoldia MacLennan]. Oliver & Boyd, Edinburgh limatula and Nucula delphinodonta as arising in the ex­ Bernard, F. R. (1980). A new Solemya S. str. from the northeastern treme posterior region of the mantle cavity, whereas in Pacific (Bivalvia: Cryptodonta). Venus, Kyoto 39: 17-23 S. reidi gill buds arise in the mid-posterior region of the Bullock, T. H., Horridge, G. A. (1965). Structure and function in mantle cavity (Figs. 14, 37). Gill buds in both S. reidi and the nervous system of invertebrates, Vol. II. W. H. Freeman, San Francisco the Nuculoida are first detected following metamorphosis Cranfield, H. J. (1973). A study of the morphology, ultrastructure and are poorly developed at this early stage. The gill buds and histochemistry of the foot of the pediveliger of Ostrea must migrate dorsally and medially to assume the adult edulis. Mar. BioI. 22: 187-202 orientation, suspended from the roof of the posterior D' Asaro, C. N. (1967). The morphology of larval and postlarval Chione cancel/ata Linne (Eularnellibranchia: Veneridae) mantle chamber by the ctenidial septa (see Reid 1980, his reared in the laboratory. Bull. mar. sci. Gulf Caribb. 17: Fig. 5, for proper orientation of adult gill and hypo­ 949-972 branchial gland). Drew, G. A. (1897). Notes on the embryology, anatomy, and habits of Yoldia limatula, Say. Johns Hopkins Univ. Circ. 17: 11-14 Drew, G. A. (I899a). The anatomy, habits, and embryology of Nervous system Yoldia Iimatula, Say, Mem. bioI. Lab, Johns Hopkins Univ. 4: 1-37 It is uncertain whether cerebral ganglia of Solemya reidi Drew, G. A. (I899b) Some observations on the habits, anatomy are derived from the three pairs of unciliated cells on the and embryology of members of the Protobranchia. Anal. Anz. 15: 493-519 test surface (see Gustafson and Reid 1986) or directly from Drew, G. A. (1901). The life history of Nucula delphinodonta the quartet of apical plate cells (Figs. 41, 42). Although the (Mighels). Q. J. microsc, Sci, 44: 313-391 three pairs of unciliated cells correspond in number with Elston, R. (1980). Functional anatomy, histology and ul­ the three paired ganglia of bivalves (Bullock and Horridge trastructure of the soft tissues of the larval American oyster, 1965) and bear striking resemblance to nervous-system Crassostrea virginica. Proc. natn, Shellfish. Ass. 70: 65-93 Gureeva, M. A., Ivanov, A. V. (1986). On the coelomic mesoderm rudiments in aplacophoran larvae (Thompson 1960), the formation in embryos of Oligobrachia mashikoi (Pogono­ pedal and visceral ganglia in both lamellibranchs and pro­ phora). Zool. Zh. 65: 780-788 tobranchs are purported to arise from epithelial thicken­ Gustafson, R. G., Reid, R. G. B. (1986). Development of the peri­ ings of the foot epithelium and the posterior mantle epi­ calymma larva of Solemya reidi (Bivalvia: Cryptodonta: Solemyidae) as revealed by light and electron microscopy. thelium, respectively. Thickenings on the foot of S. reidi Mar. BioI. 93: 411-427 may represent pedal ganglia (Fig. 28). Beklemishev (1969, Hampson, G. R. (1971). A species pair of the genus Nucula (Bi­ p. 90) emphasized development of the cerebral ganglia in valvia) from the eastern coast of the United States. Proc. malac. molluscs from four radial brain rudiments of the apical Soc. Lond.39: 333-342 plate. Cleavage in S. reidi produces an anterior quartet of Ivanov, A. V. (1963). Pogonophora. Academic Press, New York Jouin, C. (1979). Description of a free-living polychaete without cells, derived equally from the four cleavage quadrants, gut: Astomus taenioides n. gen., n. sp. (Protodrilidae, Ar­ which invaginate and come to lie immediately below the chiannelida). Can. J. Zool. 57: 2448-2456 R. G. Gustafson and R. G. B. Reid: Gutless bivalve morphogenesis 387

Kuznetsov. A P., Shileiko, A A (1984). Gutless Protobranchia Reid, R. G. B., Bernard, F. R. (1980). Gutless bivalves. Science, (Bivalvia). BioI. Nauki (Mosk) 0 (2): 39-49 N.Y. 208: 609-610 Lane, D. J. w., Nott, J. A (1975). A study of the morphology, fine Reid, R. G. B., Brand, D. G. (1987). Observations on Australian structure and histochemistry of the foot of the pediveliger of Solemyidae. J. Aust. malac. Soc. 8: 41-50 Mvtilus edulis L. J. mar. bioI. Ass. U.K. 55: 477-495 Richards, K. L., Fleming, T. P.. Jamieson, B. G. M. (1982). An ul­ Lane: D. J. W., Nott, J. A, Crisp, D. J. (1982). Enlarged stem trastructural study of the distal epidermis and the occurrence glands in the foot of the post-larval mussel Mytilus edulis: of subcuticular bacteria in the gutless tubificid Phallodrilus al­ adaptation for bysso-pelagic migration. J. mar. bioI. Ass. U.K. bidus (Oligochaeta: Annelida). Aust. J. Zool. 30: 327-336 62: 809-818 Sternpell, W. (1899). Zur Anatomie von Solemya logata Polio Zool. Morton, B. S. (1977). The hypobranchial gland in the Bivalvia. Jb. (Abt. Anat. Ont. Tiere) 13: 89-170 Can. J. ZooI. 55: 1225-1234 Thompson, T. E. (1960). The development of Neomenia carinata Ott. J.. Rieger, G., Rieger, R., Endercs. F. (1982). New mouthless Tullberg (Mollusca Aplacophora). Proc. R. Soc. (Ser. B) 153: interstitial worms from the sulfide system: symbiosis with pro­ 263-278 karyotes. Pubbl. Staz. zool. Napoli (T: Mar. Ecol.) 3: 313-333 Yonge. C. M. (1939). The protobranchiate Mollusca: A functional Owen, G. (1959). The ligament and digestive system in the taxo­ interpretation of their structure and evolution. Phil. Trans. R. dont bivalves. Proc. malac. Soc. Lond. 33: 215-223 Soc. (Ser. B) 230: 79-147 Owen. G. (1961). A note on the habits and nutrition of Solemva Yonge, C. M. (1962). On the primitive significance of the byssus in parkinson! (Protobranchia: Bivalvia). Q. JI microsc. Sci. 102: the Bivalvia and its effects in evolution. J. mar. biol. Ass. U.K. 15-21 42: 113-125 Pelseneer. P. (1891). Contribution a l'etude des lamellibranches. Archs. BioI.. Paris II: 147-312 Raven, C. P. (1966). Morphogenesis. The analysis of molluscan development. Pergamon Press, Oxford Reid, R. G. B. (1980). Aspects of the biology of a gutless species of Date offinal manuscript acceptance: November 6, 1987. Solemya (Bivalvia: Protobranchia). Can. J. ZooI. 58: 386-393 Communicated by J. M. Lawrence. Tampa

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